Islands and Stepping-Stones: Comparative Population Structure of Anopheles gambiae sensu stricto and Anopheles arabiensis in Tanzania and Implications for the Spread of Insecticide Resistance

Abstract

Population genetic structures of the two major malaria vectors Anopheles gambiae s.s. and An. arabiensis, differ markedly across Sub-Saharan Africa, which could reflect differences in historical demographies or in contemporary gene flow. Elucidation of the degree and cause of population structure is important for predicting the spread of genetic traits such as insecticide resistance genes or artificially engineered genes. Here the population genetics of An. gambiae s.s. and An. arabiensis in the central, eastern and island regions of Tanzania were compared. Microsatellite markers were screened in 33 collections of female An. gambiae s.l., originating from 22 geographical locations, four of which were sampled in two or three years between 2008 and 2010. An. gambiae were sampled from six sites, An. arabiensis from 14 sites, and both species from two sites, with an additional colonised insectary sample of each species. Frequencies of the knock-down resistance (kdr) alleles 1014S and 1014F were also determined. An. gambiae exhibited relatively high genetic differentiation (average pairwise FST = 0.131), significant even between nearby samples, but without clear geographical patterning. In contrast, An. arabiensis exhibited limited differentiation (average FST = 0.015), but strong isolation-by-distance (Mantel test r = 0.46, p = 0.0008). Most time-series samples of An. arabiensis were homogeneous, suggesting general temporal stability of the genetic structure. An. gambiae populations from Dar es Salaam and Bagamoyo were found to have high frequencies of kdr 1014S (around 70%), with almost 50% homozygote but was at much lower frequency on Unguja Island, with no. An. gambiae population genetic differentiation was consistent with an island model of genetic structuring with highly restricted gene flow, contrary to An. arabiensis which was consistent with a stepping-stone model of extensive, but geographically-restricted gene flow.

Assessing connectivity despite high diversity in island populations of a malaria mosquito

“…Understanding the population genetics of island Anopheles gambiae has both evolutionary and practical importance. A limited number of genetic investigations have been conducted on oceanic [29–32] and lacustrine islands [33–36], though the latter have been limited in the type or count of molecular markers used. In contrast to shallow population structure across Africa [4, 5], partitioning of genetic variation on islands suggests varying isolation.…”

Investigating associations between biting time in the malaria vector Anopheles arabiensis Patton and single nucleotide polymorphisms in circadian clock genes: support for sub-structure among An. arabiensis in the Kilombero valley of Tanzania

“…arabiensis at the village-level in the Kilombero Valley, indicating this species exists in genetically distinct populations between villages situated only 40 km apart [ 63 ]. However in a recent study [ 72 ], An. arabiensis from the Kilombero Valley were predicted to exist within a single population including others from coastal Tanzania and the islands of Zanzibar.…”

Spatio-temporal genetic structure of Anopheles gambiae in the Northwestern Lake Victoria Basin, Uganda: implications for genetic control trials in malaria endemic regions

“…Although passive migration through the upper airstream or hitchhiking with human transport are possible [ 8 , 22 ], indirect genetic evidence supports substantial isolation imposed by the ocean, given sufficient distance between the continent and an oceanic island. Based on microsatellites or small-scale single nucleotide polymorphism (SNP) arrays, differentiation between mainland and oceanic islands is negligible or slight at distances of 50–100 km ( F ST : 0–0.02) ([ 19 , 20 ], but see [ 23 ]) but progressively stronger at distances of 300–400 km ( F ST : 0–0.05) [ 21 ] and 600–800 km ( F ST : ~ 0.2) [ 20 ].…”